Differential early subcortical involvement in genetic FTD within the GENFI cohort.


Journal

NeuroImage. Clinical
ISSN: 2213-1582
Titre abrégé: Neuroimage Clin
Pays: Netherlands
ID NLM: 101597070

Informations de publication

Date de publication:
2021
Historique:
received: 12 01 2021
revised: 08 03 2021
accepted: 23 03 2021
pubmed: 26 4 2021
medline: 31 7 2021
entrez: 25 4 2021
Statut: ppublish

Résumé

Studies have previously shown evidence for presymptomatic cortical atrophy in genetic FTD. Whilst initial investigations have also identified early deep grey matter volume loss, little is known about the extent of subcortical involvement, particularly within subregions, and how this differs between genetic groups. 480 mutation carriers from the Genetic FTD Initiative (GENFI) were included (198 GRN, 202 C9orf72, 80 MAPT), together with 298 non-carrier cognitively normal controls. Cortical and subcortical volumes of interest were generated using automated parcellation methods on volumetric 3 T T1-weighted MRI scans. Mutation carriers were divided into three disease stages based on their global CDR® plus NACC FTLD score: asymptomatic (0), possibly or mildly symptomatic (0.5) and fully symptomatic (1 or more). In all three groups, subcortical involvement was seen at the CDR 0.5 stage prior to phenoconversion, whereas in the C9orf72 and MAPT mutation carriers there was also involvement at the CDR 0 stage. In the C9orf72 expansion carriers the earliest volume changes were in thalamic subnuclei (particularly pulvinar and lateral geniculate, 9-10%) cerebellum (lobules VIIa-Crus II and VIIIb, 2-3%), hippocampus (particularly presubiculum and CA1, 2-3%), amygdala (all subregions, 2-6%) and hypothalamus (superior tuberal region, 1%). In MAPT mutation carriers changes were seen at CDR 0 in the hippocampus (subiculum, presubiculum and tail, 3-4%) and amygdala (accessory basal and superficial nuclei, 2-4%). GRN mutation carriers showed subcortical differences at CDR 0.5 in the presubiculum of the hippocampus (8%). C9orf72 expansion carriers show the earliest and most widespread changes including the thalamus, basal ganglia and medial temporal lobe. By investigating individual subregions, changes can also be seen at CDR 0 in MAPT mutation carriers within the limbic system. Our results suggest that subcortical brain volumes may be used as markers of neurodegeneration even prior to the onset of prodromal symptoms.

Sections du résumé

BACKGROUND
Studies have previously shown evidence for presymptomatic cortical atrophy in genetic FTD. Whilst initial investigations have also identified early deep grey matter volume loss, little is known about the extent of subcortical involvement, particularly within subregions, and how this differs between genetic groups.
METHODS
480 mutation carriers from the Genetic FTD Initiative (GENFI) were included (198 GRN, 202 C9orf72, 80 MAPT), together with 298 non-carrier cognitively normal controls. Cortical and subcortical volumes of interest were generated using automated parcellation methods on volumetric 3 T T1-weighted MRI scans. Mutation carriers were divided into three disease stages based on their global CDR® plus NACC FTLD score: asymptomatic (0), possibly or mildly symptomatic (0.5) and fully symptomatic (1 or more).
RESULTS
In all three groups, subcortical involvement was seen at the CDR 0.5 stage prior to phenoconversion, whereas in the C9orf72 and MAPT mutation carriers there was also involvement at the CDR 0 stage. In the C9orf72 expansion carriers the earliest volume changes were in thalamic subnuclei (particularly pulvinar and lateral geniculate, 9-10%) cerebellum (lobules VIIa-Crus II and VIIIb, 2-3%), hippocampus (particularly presubiculum and CA1, 2-3%), amygdala (all subregions, 2-6%) and hypothalamus (superior tuberal region, 1%). In MAPT mutation carriers changes were seen at CDR 0 in the hippocampus (subiculum, presubiculum and tail, 3-4%) and amygdala (accessory basal and superficial nuclei, 2-4%). GRN mutation carriers showed subcortical differences at CDR 0.5 in the presubiculum of the hippocampus (8%).
CONCLUSIONS
C9orf72 expansion carriers show the earliest and most widespread changes including the thalamus, basal ganglia and medial temporal lobe. By investigating individual subregions, changes can also be seen at CDR 0 in MAPT mutation carriers within the limbic system. Our results suggest that subcortical brain volumes may be used as markers of neurodegeneration even prior to the onset of prodromal symptoms.

Identifiants

pubmed: 33895632
pii: S2213-1582(21)00090-5
doi: 10.1016/j.nicl.2021.102646
pmc: PMC8099608
pii:
doi:

Substances chimiques

C9orf72 Protein 0
Progranulins 0
tau Proteins 0

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

102646

Subventions

Organisme : Medical Research Council
ID : MR/M008525/1
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 103838
Pays : United Kingdom
Organisme : Medical Research Council
ID : MC_UU_00024/1
Pays : United Kingdom
Organisme : NIMH NIH HHS
ID : RF1 MH123195
Pays : United States
Organisme : CIHR
Pays : Canada
Organisme : Medical Research Council
ID : MR/T046015/1
Pays : United Kingdom
Organisme : Department of Health
ID : BRC149/NS/MH
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/K010395/1
Pays : United Kingdom
Organisme : Wellcome Trust
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/M023664/1
Pays : United Kingdom

Investigateurs

Sónia Afonso (S)
Maria Rosario Almeida (M)
Sarah Anderl-Straub (S)
Christin Andersson (C)
Anna Antonell (A)
Silvana Archetti (S)
Andrea Arighi (A)
Mircea Balasa (M)
Myriam Barandiaran (M)
Nuria Bargalló (N)
Robart Bartha (R)
Benjamin Bender (B)
Alberto Benussi (A)
Maxime Bertoux (M)
Anne Bertrand (A)
Valentina Bessi (V)
Sandra Black (S)
Sergi Borrego-Ecija (S)
Jose Bras (J)
Alexis Brice (A)
Rose Bruffaerts (R)
Agnès Camuzat (A)
Marta Cañada (M)
Valentina Cantoni (V)
Paola Caroppo (P)
Miguel Castelo-Branco (M)
Olivier Colliot (O)
Thomas Cope (T)
Vincent Deramecourt (V)
María de Arriba (M)
Giuseppe Di Fede (G)
Alina Díez (A)
Diana Duro (D)
Chiara Fenoglio (C)
Camilla Ferrari (C)
Catarina B Ferreira (CB)
Nick Fox (N)
Morris Freedman (M)
Giorgio Fumagalli (G)
Aurélie Funkiewiez (A)
Alazne Gabilondo (A)
Roberto Gasparotti (R)
Serge Gauthier (S)
Stefano Gazzina (S)
Giorgio Giaccone (G)
Ana Gorostidi (A)
Caroline Greaves (C)
Rita Guerreiro (R)
Carolin Heller (C)
Tobias Hoegen (T)
Begoña Indakoetxea (B)
Vesna Jelic (V)
Hans-Otto Karnath (HO)
Ron Keren (R)
Gregory Kuchcinski (G)
Tobias Langheinrich (T)
Thibaud Lebouvier (T)
Maria João Leitão (M)
Albert Lladó (A)
Gemma Lombardi (G)
Sandra Loosli (S)
Carolina Maruta (C)
Simon Mead (S)
Lieke Meeter (L)
Gabriel Miltenberger (G)
Rick van Minkelen (R)
Sara Mitchell (S)
Katrina Moore (K)
Benedetta Nacmias (B)
Annabel Nelson (A)
Jennifer Nicholas (J)
Linn Öijerstedt (L)
Jaume Olives (J)
Sebastien Ourselin (S)
Alessandro Padovani (A)
Jessica Panman (J)
Janne M Papma (JM)
Yolande Pijnenburg (Y)
Cristina Polito (C)
Enrico Premi (E)
Sara Prioni (S)
Catharina Prix (C)
Rosa Rademakers (R)
Veronica Redaelli (V)
Daisy Rinaldi (D)
Tim Rittman (T)
Ekaterina Rogaeva (E)
Adeline Rollin (A)
Pedro Rosa-Neto (P)
Giacomina Rossi (G)
Martin Rossor (M)
Beatriz Santiago (B)
Dario Saracino (D)
Sabrina Sayah (S)
Elio Scarpini (E)
Sonja Schönecker (S)
Elisa Semler (E)
Rachelle Shafei (R)
Christen Shoesmith (C)
Imogen Swift (I)
Miguel Tábuas-Pereira (M)
Mikel Tainta (M)
Ricardo Taipa (R)
David Tang-Wai (D)
Paul Thompson (P)
Hakan Thonberg (H)
Carolyn Timberlake (C)
Pietro Tiraboschi (P)
Philip Van Damme (P)
Mathieu Vandenbulcke (M)
Michele Veldsman (M)
Ana Verdelho (A)
Jorge Villanua (J)
Jason Warren (J)
Carlo Wilke (C)
Ione Woollacott (I)
Elisabeth Wlasich (E)
Henrik Zetterberg (H)
Miren Zulaica (M)

Informations de copyright

Copyright © 2021 The Author(s). Published by Elsevier Inc. All rights reserved.

Auteurs

Martina Bocchetta (M)

Dementia Research Centre, Department of Neurodegenerative Disease, UCL Queen Square Institute of Neurology, University College London, London, United Kingdom.

Emily G Todd (EG)

Dementia Research Centre, Department of Neurodegenerative Disease, UCL Queen Square Institute of Neurology, University College London, London, United Kingdom.

Georgia Peakman (G)

Dementia Research Centre, Department of Neurodegenerative Disease, UCL Queen Square Institute of Neurology, University College London, London, United Kingdom.

David M Cash (DM)

Dementia Research Centre, Department of Neurodegenerative Disease, UCL Queen Square Institute of Neurology, University College London, London, United Kingdom; Centre for Medical Image Computing, Department of Medical Physics and Biomedical Engineering, University College London, London, United Kingdom.

Rhian S Convery (RS)

Dementia Research Centre, Department of Neurodegenerative Disease, UCL Queen Square Institute of Neurology, University College London, London, United Kingdom.

Lucy L Russell (LL)

Dementia Research Centre, Department of Neurodegenerative Disease, UCL Queen Square Institute of Neurology, University College London, London, United Kingdom.

David L Thomas (DL)

Dementia Research Centre, Department of Neurodegenerative Disease, UCL Queen Square Institute of Neurology, University College London, London, United Kingdom; Neuroradiological Academic Unit, UCL Queen Square Institute of Neurology, University College London, London, United Kingdom.

Juan Eugenio Iglesias (J)

Centre for Medical Image Computing, Department of Medical Physics and Biomedical Engineering, University College London, London, United Kingdom; Martinos Center for Biomedical Imaging, Massachusetts General Hospital and Harvard Medical School, USA; Computer Science and Artificial Intelligence Laboratory, Massachusetts Institute of Technology, USA.

John C van Swieten (JC)

Department of Neurology and Alzheimer Center, Erasmus Medical Center Rotterdam, the Netherlands.

Lize C Jiskoot (LC)

Department of Neurology and Alzheimer Center, Erasmus Medical Center Rotterdam, the Netherlands.

Harro Seelaar (H)

Department of Neurology and Alzheimer Center, Erasmus Medical Center Rotterdam, the Netherlands.

Barbara Borroni (B)

Centre for Neurodegenerative Disorders, Neurology Unit, Department of Clinical and Experimental Sciences, University of Brescia, Brescia, Italy.

Daniela Galimberti (D)

Department of Biomedical, Surgical and Dental Sciences, University of Milan, Milan, Italy; Fondazione IRCCS Ca' Granda, Ospedale Maggiore Policlinico, Milan, Italy.

Raquel Sanchez-Valle (R)

Neurology Department, Hospital Clinic, Institut d'Investigacions Biomèdiques, Barcelona, Spain.

Robert Laforce (R)

Clinique Interdisciplinaire de Mémoire, Département des Sciences Neurologiques, CHU de Québec, Faculté de Médecine, Université Laval, Québec, Canada.

Fermin Moreno (F)

Hospital Universitario Donostia, San Sebastian, Spain.

Matthis Synofzik (M)

Department of Cognitive Neurology, Center for Neurology, Hertie-Institute for Clinical Brain Research, Tübingen, Germany.

Caroline Graff (C)

Karolinska Institutet, Department NVS, Division of Neurogeriatrics, Stockholm, Sweden; Unit for Hereditray Dementia, Theme Aging, Karolinska University Hospital-Solna Stockholm Sweden.

Mario Masellis (M)

Campbell Cognitive Neurology Research Unit, Sunnybrook Research Institute, Toronto, ON, Canada.

Maria Carmela Tartaglia (M)

Toronto Western Hospital, Tanz Centre for Research in Neurodegenerative Disease, Toronto, ON, Canada.

James B Rowe (JB)

Department of Clinical Neurosciences and Cambridge University Hospitals NHS Trust and Medical Research Council Cognition and Brain Sciences Unit, University of Cambridge, Cambridge, United Kingdom.

Rik Vandenberghe (R)

Laboratory for Cognitive Neurology, Department of Neurosciences, KU Leuven, Leuven, Belgium.

Elizabeth Finger (E)

Department of Clinical Neurological Sciences, University of Western Ontario, London, ON, Canada.

Fabrizio Tagliavini (F)

Fondazione Istituto di Ricovero e Cura a Carattere Scientifico, Istituto Neurologico Carlo Besta, Milan, Italy.

Alexandre de Mendonça (A)

Faculty of Medicine, University of Lisbon, Lisbon, Portugal.

Isabel Santana (I)

Neurology Department, Centro Hospitalar e Universitário de Coimbra, Portugal.

Chris R Butler (CR)

Department of Clinical Neurology, University of Oxford, Oxford, United Kingdom.

Simon Ducharme (S)

Department of Neurology and Neurosurgery, McGill University, Montreal, Quebec, Canada.

Alexander Gerhard (A)

Division of Neuroscience and Experimental Psychology, Wolfson Molecular Imaging Centre, University of Manchester, Manchester, United Kingdom; Departments of Geriatric Medicine and Nuclear Medicine, University of Duisburg-Essen, Germany.

Adrian Danek (A)

Neurologische Klinik und Poliklinik, Ludwig-Maximilians-Universität, Munich German Center for Neurodegenerative Diseases (DZNE), Munich Munich Cluster of Systems Neurology, Munich, Germany.

Johannes Levin (J)

Neurologische Klinik und Poliklinik, Ludwig-Maximilians-Universität, Munich German Center for Neurodegenerative Diseases (DZNE), Munich Munich Cluster of Systems Neurology, Munich, Germany.

Markus Otto (M)

Department of Neurology, University Hospital Ulm, Ulm, Germany.

Sandro Sorbi (S)

Department of Neuroscience, Psychology, Drug Research and Child Health, University of Florence, Florence, Italy.

Isabelle Le Ber (I)

Sorbonne Université, Paris Brain Institute - Institut du Cerveau- ICM, Inserm U1127, CNRS UMR 7225, AP-HP - Hôpital Pitié-Salpêtrière, Paris, France; Centre deréférence des démences rares ou précoces, IM2A, Département de Neurologie, AP-HP - Hôpital Pitié-Salpêtrière, Paris, France; Département de Neurologie, AP-HP - Hôpital Pitié-Salpêtrière, Paris, France.

Florence Pasquier (F)

Univ Lille, France; Inserm 1172 Lille, France; CHU, CNR-MAJ, Labex Distalz, LiCENDLille, France.

Jonathan D Rohrer (JD)

Dementia Research Centre, Department of Neurodegenerative Disease, UCL Queen Square Institute of Neurology, University College London, London, United Kingdom. Electronic address: j.rohrer@ucl.ac.uk.

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